Paranybelinia otobothrioides (Dollfus, 1966)

Morales-Ávila, José Raúl, Gómez-Gutiérrez, Jaime, Hernandez-Saavedra, Norma Y., Robinson, Carlos J. & Palm, Harry W., 2019, Phylogenetic placement and microthrix pattern of Paranybelinia otobothrioides Dollfus, 1966 (Trypanorhyncha) from krill Nyctiphanes simplex Hansen, 1911, International Journal for Parasitology: Parasites and Wildlife 10, pp. 138-148 : 147

4.4. Phylogenetic placement of Paranybelinia otobothrioides

The ssrDNA analysis of the trypanorhynch relationships including the new sequence of Pa. otobothrioides was consistent with results previously reported in studies based on concatenated ribosomal markers (e.g. Palm et al., 2009). The superfamily Eutetrarhynchoidea appeared paraphyletic. It comprises four clades, remaining the family relationships within the superfamily unresolved. The Prochristianella / Parachristianella / Trimacracanthus / clade together with the nested Mixodigmatidae ( Trygonicola / Halysiorhynchus ) combines genera with 2 and 4 bothria, the former with a heteroacanthous typical and the Mixodigmatidae with a poeciloacanthous armature. The species Hispidorhynchus australiensis represents a second clade with 2 bothria and a heteroacanthous homeocanthous armature sister to the Tetrarhynchobothrium / Dollfusiella / Paroncomegas clade and the phylogenetically derived clade Mecistobothrium / Oncomegas that unite heteroacanthous and homeocanthous species with 2 bothria.

A further trypanorhynch clade included species with 4 bothria before placement of Pa. otobothrioides in the present study ( Palm et al., 2009). That phylogenetic hypothesis placed the heteroacanthous Rhinoptericola megacantha with 4 bothria and prebulbar organs ( Rhinoptericolidae ) together with Nataliella marcelli Palm, 2010 (4 bothria, homeoacanthous, prebulbar organs, also Rhinoptericolidae in Palm, 2010) in a clade with the mainly homeoacanthous tentaculariids, intermediate between a subgroup of the paraphyletic ‘eutetrarhynchoids’ and the tentacularioids ( Palm et al., 2009). Paranybellinia otobothrioides positioned inside the clade with the Rhinoptericolidae (Eutetrarhynchoidea) and the Tentaculariidae (Tentacularioidea) . However, with its characteristic scolex morphology, surface ultrastructure and the muscular rings around the tentacle sheaths instead of prebulbar organs, Pa. otobothrioides is clearly affiliated with the Tentacularioidea and not the Eutetrarhynchoidea .

Having 2 bothria instead of 4, Pa. otobothrioides forms a distinct clade sister to the species representing the family Tentaculariidae . This result concurs with the hypothesis originally proposed by cladistic analyses which demonstrated a close relationship of the family Paranybeliniidae with the Tentaculariidae ( Campbell and Beveridge, 1994; Beveridge et al., 1999); and with the transfer of the Paranybeliniidae into the Tentacularioidea based on scolex morphology and surface ultrastructure as suggested by Palm (2008). The sister-group relationship between Pa. otobothrioides and the Tentaculariidae also strongly supports the monophyly of the superfamily Tentacularioidea as proposed by Palm et al. (2009).

Genetic distance has been used as an important indicator for species discrimination (e.g. Haseli et al., 2017), ranging between allopatric conspecifics in members of the Eutetrarhynchidae (0.22%–1.66%), Tentacularioidea (0.00%–0.11%), Gymnorhynchoidea (0.00%–0.08%) and Lacistorhynchoidea (0.00%–0.33%) ( Palm et al., 2007, 2009). To date, there is no genetic distance threshold to distinguish family boundaries inside the Trypanorhyncha . However, the genetic distance values observed between Pa. otobothrioides and the Tentaculariidae (average K2P = 0.033 [3.3%]; Table 2) could be consistent with that observed among monophyletic superfamiles. The low degree of divergence of the ssrDNA analyzed fragment most likely reflects species that are delimited by more subtle morphological traits. Based on the average K2P observed between the Tentacularioidea , which is supported by several differences in morphological features of Pa. otobothrioides (e.g. 2 bothria [not entirely split into 4 bothria, see Fig. 2a–c , Fig. 3a ,] with free lateral and posterior margins, 4 posterior tegumental grooves, and hamulate mictotriches on the entire distal bothrial surface) together with the characteristic blastocysts inside euphausiids as second intermediate hosts, we therefore maintain the Paranybeliniidae as an own family within the Tentacularioidea , necessitating emendation of the superfamily diagnosis in the most recent classification by Palm (2004).

Figures

Fig. 2. Surface ultrastructure of the scolex and tentacular armature of Pa. otobothrioides. (A) Dorso-ventral view of the scolex dissected from the blastocyst showing the distal bothrial surface without complete median separation. (B) Pedunculus scolecis showing 2 bothria with free lateral and posterior margins. (C) Apical view of the scolex bothrial surfaces. (D) Capilliform filitriches. (E) External tentacle surface, metabasal armature with solid uncinate hooks. (F) Distal bothrial surface showing (G) hamulate spinitriches and (H) lineate spinitriches. Scale bars: (A,C) 100 μm; (D–H) 50 μm.

Fig. 3. Paranybelinia otobothrioides anatomy showing details of the bothria (Bo), tentacles (Te), appendix (Ap), bulbs (Bu), and velum (Ve). The arrows show the muscular rings surrounding the tentacle sheaths. Scale = 60 μm.